Hybridization between <Emphasis Type="Italic">Alouatta caraya</Emphasis> and <Emphasis Type="Italic">Alouatta guariba clamitans</Emphasis> in captivity

Hybridization between Alouatta spp. has been suggested at contact zones of A. palliata and A. pigra in Mexico and of A. caraya and A. guariba clamitans in Brazil and Argentina. Whereas genetic data confirmed hybridization between the former pair of species, hybrid individuals of the latter pair have been putatively identified on the basis of a mosaic pelage color. In this paper, we describe the first confirmed cases of hybridization between a female A. guariba clamitans and a male A. caraya. One hybrid male was born in 2007 and one hybrid female was born in 2009 with distinct coat colors. The male resembled the newborn color pattern characteristic of A. guariba clamitans, whereas the female resembled the newborn pattern of A. caraya. The birth and survival of the male hybrid for a year and a half indicated the viability of the heterogametic sex.     

Morphometric and morphologic parameters of the heart in healthy Alouatta guariba clamitans (Cabrera, 1940)

Background

This study aimed at assessing the heart function of one neotropical primate (Alouatta guariba clamitans) kept in captivity using radiography, electrocardiogram (ECG) and Doppler echocardiography.

Methods

Ten adult healthy howler monkeys (A. g. clamitans) were evaluated under general anaesthesia. Vertebral Heart Scores (VHS) were obtained from radiographic studies. Ejection fraction, shortening fraction of left ventricle, left atrial/aortic root ratio, ascending aortic diameter, peak velocity of pulmonary, mitral, tricuspid and aortic blood flow and other values were measured by Doppler echocardiography. Heart rate, mean electrical axis of QRS complex, P, Q, R, S, T amplitude, P, PR interval, QRS, QT interval duration and ST segment unbalancing were measured by ECG.

Results and conclusions

Exam techniques were akin the ones used in humans. Doppler echocardiographic, radiographic, electrocardiographic and clinical parameters for howler monkey were described and correlated. The results have shown profiles of cardiovascular function and structure of A. g. clamitans.     

Bacterial endocarditis and increased cardiac troponin I levels in a brown howler monkey (Alouatta guariba clamitans) with an interventricular septal defect

A brown howler monkey (Alouatta guariba clamitans) was presented with lethargy, hyporexia, cough and heart murmur. The complementary tests and necropsy revealed pleuropneumonia, bacterial endocarditis and interventricular septal defect. To the best of our knowledge, this is the first report of increased cardiac troponin I levels in this species.     

Capture of Alouatta guariba clamitans for the surveillance of sylvatic yellow fever and zoonotic malaria: Which is the best strategy in the tropical Atlantic Forest?

Howler monkey capture is an arduous and expensive task requiring trained and specialized professionals. We compared strategies and methods to most efficiently capture Alouatta guariba clamitans in remnants of the Atlantic Forest in Rio de Janeiro and its bordering states of Minas Gerais and São Paulo. We tested whether or not the success of expeditions in the forest with anesthetic darts, nets, and baited traps differed with and without the support of an information network, a contact chain built with key institutions and inhabitants to continuously monitor howler monkey presence. The influence of forest conditions (vegetation type and fragment size) upon darting success was also evaluated. We captured 24 free‐living A. guariba clamitans. No howler monkey was caught with traps, probably due to the predominantly folivore feeding to high local plant diversity providing a great variety of food options. Captures based on an information network were significantly more efficient in terms of numbers of caught monkeys than without it. Captures with darts were considerably more efficient when performed in semideciduous forests and small forest fragments as opposed to ombrophilous forests or large woods. Although we walked great distances within the forest searching for howler monkeys, all but one animal were captured at the forest fringes. Hindrances to search and the darting method in the Atlantic Forest, for example, the steep terrain, high tree canopies, hunt pressure, and low A. guariba clamitans population density, were mitigated with the use of the information network in this monkey capture. Moreover, the information network enhanced the surveillance of zoonotic diseases, which howler monkeys and other nonhuman primates are reservoirs in Brazil, such as malaria and yellow fever.     

Fibular and metatarsal osteosynthesis in a southern brown howler monkey (Alouatta guariba clamitans)

Here we describe a successful surgical management of a distal fibular fracture combined with a tarsocrural luxation and multiple metatarsal fractures in the left foot of a southern brown howler monkey (Alouatta guariba clamitans). We achieved satisfactory outcome by applying intramedullary pinning for each of the bone fractures and closed reduction of joint luxation—kept in place only by bone alignment, without further ligament reconstruction. Bone healing occurred uneventfully within eight weeks and the monkey's foot regained its normal function. Therefore, we could properly release the patient back into the wild.     

Transverse lie with prolapsed arm in a female red‐howler monkey (Alouatta guariba clamitans – Cabrera, 1940)

This study focuses on a case of a red‐howler monkey (Alouatta guariba clamitans) which was found with a fetus in a transverse lie position with a prolapsed arm. The topic of this research is well justified as there are no data on this condition involving this type of non‐human primate in literature. In this study, a red‐howler monkey was observed by locals pulling at her pelvic region for 3 days near a farm. On the third day, the monkey was found lying on the ground at which point she offered no resistance when approached. The environmental police took the monkey to receive medical attention. During the physical examination, it was quickly observed that the monkey was pregnant; the right forelimb of the fetus was exposed from the vulva. An ultrasound revealed a non‐viable fetus, and due to the severe weakness of the mother, we opted for euthanasia. During the necropsy, not only was the fetus found macerated but it was also in a transverse lie position with a prolapsed arm and presented no external or internal injuries consistent with trauma.     

Attacks of domestic dogs on Common Long-Nosed Armadillo Dasypus novemcinctus and Southern Brown Howler Monkey Alouatta guariba in fragmented Atlantic Forest and implications in a region of high priority for biodiversity conservation

Domestic dogs can negatively impact natural systems, and understanding these dynamics is essential to mitigate their impact. We report two cases of attacks of domestic dogs on native mammals in a fragmented landscape of the Atlantic Forest, southern Brazil. Our records occurred in a region of high priority for the conservation of this biome. We observed two attacks, one on a Common Long-Nosed Armadillo Dasypus novemcinctus and another on a Southern Brown Howler Monkey Alouatta guariba clamitans. Our records highlight additional threats to the wild and native fauna reinforcing the importance of accounting for the presence of domestic fauna when delineating conservation strategies in highly fragmented environments.     

Wild mixed groups of howler species (<Emphasis Type="Italic">Alouatta caraya</Emphasis> and <Emphasis Type="Italic">Alouatta clamitans</Emphasis>) and new evidence for their hybridization

Mixed species groups and hybridization are common among primates, yet these phenomena are rare and poorly understood for the genus Alouatta. In this study, we describe the composition of howler groups in a sympatric area of Alouatta caraya and Alouatta clamitans and provide new evidence for the occurrence of interspecific hybridization. Between October 2006 and April 2007, 11 howler groups were located in a 150-ha forest fragment: two monospecific groups of A. caraya, two monospecific groups of A. clamitans, two groups composed of A. clamitans and hybrid morphotypes (A. caraya × A. clamitans), and five groups composed of both species together with hybrid morphotypes (mixed species groups). The average size of the studied groups was 5.2 ± 1.2 individuals. Monospecific and mixed groups (mixed species groups + groups with hybrids) did not differ significantly in their sizes. In total, the sex/age ratios were 1 AM:1.5 AF:0.2 SAM:0.5 JUV:0.2 INF and the species ratios were 1 A. caraya:1.6 A. clamitans:0.4 A. caraya × A. clamitans. The ratio of immatures to 1AF was larger in the monospecific groups (0.75 immatures:1AF) than in mixed groups (0.29 immatures:1AF), possibly reflecting a lower viability in the latter. Two features of the hybrid morphotypes of the upper Paraná River support their status as true hybrids: the polymorphism of their coloration patterns and the extremely female-biased sex ratio. The effects of Haldane’s rule and population fragmentation on the interactions between both species are discussed. Contribution number 1689 of the Departamento de Zoologia, Universidade Federal do Paraná (UFPR), Caixa Postal 19020, 81531-990, Curitiba, Paraná, Brazil. Contract grant sponsor: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).     

Antipredator Behavior of Brown Howlers Attacked by Black Hawk-eagle in Southern Brazil

In field studies between 2002 and 2004 in southern Brazil, we recorded antipredatory behaviors (N=9) of brown howlers (Alouatta guariba clamitans) under attack by the black hawk-eagle (Spizaetus tyrannus). We observed 2 types of behavioral responses: the descent to the understory followed by the dispersion of the group and immobility and silence. Brown howlers displayed behaviors specific to evading aerial predators, which are similar to the ones in other Neotropical primates.The article is contribution number 1578 of Departamento de Zoologia, Universidade Federal do Paraná     

Impact of yellow fever outbreaks on two howler monkey species (Alouatta guariba clamitans and A. caraya) in Misiones,Argentina

Two yellow fever outbreaks (YFOs) ocurred in northeastern Argentina between November 2007 and October 2008, seriously affecting populations of two howler monkey species: the brown howler Alouatta guariba clamitans and the black howler Alouatta caraya. Both howlers live syntopically in El Piñalito Provincial Park, Misiones, where four groups (36 individuals) were studied since January 2005. The first dead howlers were found on January 20, 2008, in El Piñalito. Systematic searches found 14 dead howlers within the area (12 from the study groups and two from neighboring groups), with only two young seen on January 25, 2008, and none found since up to December 2008. In October 2008, another YFO hit howler monkey populations from El Soberbio, Misiones. Overall, 59 howlers were found dead in Misiones from November 2007 to December 2008. Thanks to the alert of the howler's death in El Piñalito, a prompt human vaccination campaign started in the area. Wild howler monkey populations from both species are in a delicate situation in Misiones, especially the brown howler, an already endangered species in Argentina and endemic to the Atlantic Forest. If we add the recurrence of YFOs to the reduction of suitable habitat to small fragments, it could be only a matter of time until howler populations disappear from the Upper Paraná Atlantic Forest in Misiones. Am. J. Primatol. 72:475–480, 2010. © 2010 Wiley‐Liss, Inc.     

Observations on the female internal reproductive organs of the brown howler monkey (Alouatta guariba clamitans)

Alouatta guariba clamitans (brown howler monkey) is an endemic primate from the southeastern Brazil tropical forests, classified as near threatened by the IUCN Red List 2007. The genus Alouatta is one of the most difficult New World monkeys to breed and rear in captivity. In this study we examined the macroscopic and histological aspects of the female genital tract of wild brown howler monkeys to provide baseline information for future reproduction research. The anatomical relationship between the vagina, uterus, broad ligament, oviducts and ovaries are those of a typical primate reproductive tract. The fundic portion of the uterus is globoid, the cervix is well developed, which confers to the uterus an elongated shape, and the vagina is a long flattened channel. Histological analysis conducted in females in the follicular phase revealed large quantities of interstitial luteinized tissue in the ovaries, a stratified nonkeratinized vaginal epithelium, lack of glands in the vaginal mucosa and simple tubular endometrial glands. The observed anatomical features should be considered in the adaptation and application of assisted reproductive techniques aimed at improving captive reproduction for species conservation. Am. J. Primatol. 71:145–152, 2009. © 2008 Wiley‐Liss, Inc.     

Artificial nest predation by brown howler monkeys (Alouatta guariba clamitans)

Howler monkeys (Alouatta spp.) have long been considered strongly vegetarian primates. Their occasional ingestion of invertebrates has largely been interpreted as unintentional. Recent observations of the consumption of bird eggs by Alouatta caraya living in small and resource-impoverished habitat patches in the state of Rio Grande do Sul (RS), Brazil help to confirm that such behavior by howler monkeys is at times intentional. We report the findings of an experimental study on artificial nest predation by free-ranging Alouatta guariba clamitans in RS and third-party unpublished observations of intentional feeding on animal matter by Alouatta arctoidea in Venezuela and Alouatta palliata in Mexico. A nest station composed of ten artificial nests baited daily with two quail eggs each was placed at six study sites. Each site was monitored from dawn to dusk during 10–12 consecutive days. Individuals (juvenile males and an adult female) from two of the six study groups inspected the nests and ate eggs once. Study subjects from these two groups were the only ones to be supplemented with food (basically fruit) by local inhabitants, a habit that may have decreased their level of neophobia and facilitated their visit to the artificial nests. We suggest that faunivory is an opportunistic and infrequent, but intentional howler monkey feeding behavior.     

Ovarian cycle of southern brown howler monkey (<Emphasis Type="Italic">Alouatta guariba clamitans</Emphasis>) through fecal progestin measurement

The ovarian cycle in howler monkeys (genus Alouatta) has beean investigated through several biological parameters (ranging between 16.3 and 29.5 days); however, no data exist concerning the ovarian activity of the southern brown howler monkey (Alouatta guariba clamitans). This study aimed to describe the ovarian cycle of A. g. clamitans by profiling fecal progestin concentrations. Over 20 weeks, fecal samples of eight captive adult females of A. g. clamitans were collected. The collections were made at dawn, 5 days a week, and the samples were frozen immediately following collection. Next, they were dried, pulverized and hormonal metabolites were extracted to determine progestin concentrations by enzyme immunoassay. Of the 758 samples tested, the mean concentration of fecal progestins was 2866.40 ± 470.03 ng/g of dry feces, while the mean concentration at baseline was 814.47 ± 164.36 ng/g of dry feces. Among the eight females, one showed no ovarian cyclicity and three presented periods of probable absence of cyclicity and low progestin concentrations. A mean duration of 16 ± 0.52 days was observed for the 35 cycles studied. The interluteal phase lasted 4 ± 0.37 days on average, with a mean concentration of fecal progestins of 467.98 ± 29.12 ng/g of dry feces, while the luteal phase lasted 11 ± 0.50 days, with a mean concentration of 4283.27 ± 193.31 ng/g of dry feces. Besides describing the characteristics of the ovarian cycle, possible causes for the low concentrations of fecal progestins and periods of absence of cyclicity are also discussed.     

Roaring Behavior of Two Syntopic Howler Species (Alouatta caraya and A. guariba clamitans): Evidence Supports the Mate Defense Hypothesis

Long-distance calls are loud vocalizations involved in within and between group communication in animals. These calls may maintain cohesion with group members or communicate the ownership of valuable resources such as territory, food, or mates to individuals from other groups. In howlers (Alouatta spp.), three nonmutually exclusive hypotheses suggest that the ultimate function of roaring (howling) behavior is to protect resources from neighboring groups. The space/food defense hypothesis maintains that roars are used to gain exclusive access to food; the mate defense hypothesis holds that roars ensure exclusive access to mates; and the infanticide avoidance hypothesis states that the roaring behavior serves to avoid male takeovers and infanticide. To test these three hypotheses, we conducted a study on black-and-gold howlers (Alouatta caraya) and brown howlers (A. guariba clamitans) living in syntopy at El Pi?alito provincial park in northeast Argentina. We recorded 12 mo of data on the roaring behavior of two groups of each species, along with data on food availability and diet. Although all four groups overlapped extensively in their use of food resources during the study period, roars occurred much more frequently during interactions between groups of the same species than between groups of different species. Roaring frequency was not higher during the lean season, when high-quality food was less abundant. Howlers did not roar more frequently at home range boundaries, nor were roaring bouts spatially associated with valuable feeding resources. Males participated in all of the roaring bouts, whereas females participated in only 29% of them. Adults did not roar more frequently when there were unweaned infants in the group, as expected if roaring behavior decreases infanticide risk. These results provide no support for the food defense or infanticide avoidance hypotheses, but support predictions derived from the mate defense hypothesis.     

Effects of nitrate on the interactions of the tadpoles of two ranids (Rana clamitans and R. catesbeiana)

Nitrogen pollution as a result of agricultural runoff and atmospheric deposition is a major challenge to aquatic ecosystems, and is likely to increase in the future. Nitrogenous pollutants are potential stressors of amphibian larvae through their toxicological impacts on individuals; however, they may also increase primary productivity. We examined how such an anthropogenic stressor could influence the interactions between two potentially competing species of tadpoles (Rana clamitans and R. catesbeiana). In a 42 d mesocosm experiment, R. catesbeiana survival, but not final mass, was reduced by nitrate addition. Rana catesbeiana survival was lower when in competition with R. clamitans than when only experiencing intraspecific competition. For R. clamitans, survival was not affected by nitrate addition or competition type. Rana clamitans in nitrate addition mesocosms were heavier than tadpoles from no nitrate mesocosms, and were heavier in intraspecific than in interspecific mesocosms. Our results suggest that nitrate can influence the performance of amphibian larvae, and that its effects could have complex effects on aquatic ecosystems.     

Assessing fine-scale genetic structure and relatedness in the micro-endemic Florida bog frog

The Florida bog frog (Rana okaloosae) is restricted to approximately 25 seepage drainages on the Florida Panhandle, southeastern USA. We evaluated fine-scale (<1–10 km) genetic structure among 80 samples from a long-term study area in one portion of its range. We also included co-distributed samples (N = 48) from bronze frogs (R. clamitans). Individual R. okaloosae were significantly more related to one another than expected under panmixia, though significant patterns of isolation-by-distance were detected reflecting limited dispersal. Bayesian clustering failed to identify discrete genetic clusters within species. Subtle, though important differences in genetic structuring between R. okaloosae and R. clamitans suggests that future efforts to predict the impact of landscape changes on Rana okaloosae, should focus on the species itself rather than R. clamitans as a surrogate species.     

Ocelot (Leopardus pardalis) predation on primates in Caratinga Biological Station, Southeast Brazil

This study demonstrates that ocelots (Leopardus pardalis) extensively use primates as a food resource at the Caratinga Biological Station (CBS) in Southeast Brazil. Analysis of 60 fecal samples collected over 4 years revealed predation upon the brown howler monkey (Alouatta guariba), the muriqui (Brachyteles hypoxanthus), and the brown capuchin monkey (Cebus apella). The most frequent items found in the fecal samples analyzed were Calomys (n=16) and non-identified Aves (n=15), followed by A. guariba (n=12). Although Rodentia was the most common group consumed (n=52) Primates were found in 27% of total fecal samples and were the third most consumed group in relation to the total items. Particularly, predation of A. guariba by ocelots (20% of the total fecal samples) was not an isolated event; our results showed that this species was preyed on across several months. Predation on primates was far higher at CBS than at other sites where comparable studies have been carried out.     

Intestinal helminths in wild Peruvian red uakari monkeys (Cacajao calvus ucayalii) in the northeastern Peruvian Amazon

Parasites are important in the management of the health of primate populations. We examined 36 fecal samples from Peruvian red uakari monkeys (Cacajao calvus ucayalii) collected from wild animals in the northeastern Peruvian Amazon. Samples were positive for helminth infection. Nematodes egg: Strongyloididae, Trypanoxyuris sp., Spirurid, and a cestode egg were identified.     

Sympatry between <Emphasis Type="Italic">Alouatta caraya</Emphasis> and <Emphasis Type="Italic">Alouatta clamitans</Emphasis> and the rediscovery of free-ranging potential hybrids in Southern Brazil

Records of sympatry between Alouatta caraya and A. clamitans are rare despite their extensive range overlap. An example of their current sympatry and the rediscovery of free-ranging potential hybrids of A. caraya and A. clamitans in the forests of the Upper Paraná River, Southern Brazil, are reported in this paper. Eight groups were observed in the study area: five monospecific groups of A. caraya, two of A. clamitans, and a group containing two adult males and two adult females of A. caraya and a sub-adult male and two adult females identified as Alouatta sp. The color of the last three individuals was a mosaic between the two species; this is consistent with previously described variations in museum specimens collected in the Paraná River in the 1940s that had been identified as potential hybrids. The results from this study emphasize the need for scientific studies in the region of the Ilha Grande National Park, one of the few regions in the Paraná River that currently harbors both howler species. Contribution number 1637 of the Departamento de Zoologia, Universidade Federal do Paraná, Caixa Postal 19020, 81531-980, Curitiba, Paraná, Brasil.